Diabetes-induced Proteome Changes Throughout Development

Author(s): Dina Johar*, Sara M. Ahmed, Samer El. Hayek, Nader Al-Dewik, Eshak I. Bahbah, Nabil H. Omar, Mahmoud Mustafa, Doaa O. Salman, Asmaa Fahmey, Mohamed Mottawea, Rasha A.M. Azouz, Larry Bernstein.

Journal Name: Endocrine, Metabolic & Immune Disorders - Drug Targets
(Formerly Current Drug Targets - Immune, Endocrine & Metabolic Disorders)

Volume 19 , Issue 6 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Background: Diabetes Mellitus (DM) is a multisystemic disease involving the homeostasis of insulin secretion by the pancreatic islet beta cells (β-cells). It is associated with hypertension, renal disease, and arterial and arteriolar vascular diseases.

Discussion: The classification of diabetes is identified as type 1 (gene linked β-cell destruction in childhood) and type 2 (late onset associated with β-cell overload and insulin resistance in peripheral tissues. Type 1 diabetes is characterized by insulin deficiency, type 2 diabetes by both insulin deficiency and insulin resistance. The former is a genetically programmed loss of insulin secretion whereas the latter constitutes a disruption of the homeostatic relationship between the opposing activity of β- cell insulin and alpha cell (α-cell) glucagon of the Islets of Langerhans. The condition could also occur in pregnancy, as a prenatal occurring event, possibly triggered by the hormonal changes of pregnancy combined with β-cell overload. This review discusses the molecular basis of the biomolecular changes that occur with respect to glucose homeostasis and related diseases in DM. The underlying link between pancreatic, renal, and microvascular diseases in DM is based on oxidative stress and the Unfolded Protein Response (UPR).

Conclusion: Studying proteome changes in diabetes can deepen our understanding of the biomolecular basis of disease and help us acquire more efficient therapies.

Keywords: Diabetes mellitus, proteome, organogenesis, stress signaling, unfolded protein response, endoplasmic reticulum stress.

[2]
Zhong, J. Endoplasmic reticulum (ER) stress in the pathogenesis of type 1 diabetes.In: Type 1 Diabetes; Escher, A., Ed.; , 2013.
[http://dx.doi.org/10.5772/52644]
[3]
Creager, M.A.; Lüscher, T.F.; Cosentino, F.; Beckman, J.A. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: Part I. Circulation, 2003, 108(12), 1527-1532.
[http://dx.doi.org/10.1161/01.CIR.0000091257.27563.32] [PMID: 14504252]
[4]
Ni, M.; Lee, A.S. ER chaperones in mammalian development and human diseases. FEBS Lett., 2007, 581(19), 3641-3651.
[http://dx.doi.org/10.1016/j.febslet.2007.04.045] [PMID: 17481612]
[5]
Doronzo, G.; Viretto, M.; Russo, I.; Mattiello, L.; Anfossi, G.; Trovati, M. Effects of high glucose on vascular endothelial growth factor synthesis and secretion in aortic vascular smooth muscle cells from obese and lean Zucker rats. Int. J. Mol. Sci., 2012, 13(8), 9478-9488.
[http://dx.doi.org/10.3390/ijms13089478] [PMID: 22949809]
[6]
Banting, F.; Best, C.; Collip, J.; Macleod, J. Available from: https://www.chemheritage.org/historical-profile/frederick-banting-charles-best-james-collip-and-john-macleod (Accessed Feb 17, 2019).
[7]
Minkowski, O. Discovery of the pancreatic origin of diabetes, 1889, 1989. 32, pp. 399-401
[8]
Sydney, B.H.; Robert, H.; John, E.S. The Nobel Prize in Physiol-ogy or Medicine, 2002.http://www.nobelprize.org/nobel_prizes/medicine/laureates/2002/press.html
[9]
Ciechanover, A.; Hershko, A.; Rose, I. The Nobel Prize in Chem-istry, 2004.http://www.nobelprize.org/nobel_prizes/chemistry/laureates/2004/
[10]
Ohsumi, Y. The Nobel Prize in Physiology or Medicine, 2016.https://www.nobelprize.org/nobel_prizes/medicine/laureates/2016/
[11]
Kim, S.K.; Hebrok, M. Intercellular signals regulating pancreas development and function. Genes Dev., 2001, 15(2), 111-127.
[http://dx.doi.org/10.1101/gad.859401] [PMID: 11157769]
[12]
Ozcan, L.; Tabas, I. Role of endoplasmic reticulum stress in metabolic disease and other disorders. Annu. Rev. Med., 2012, 63, 317-328.
[http://dx.doi.org/10.1146/annurev-med-043010-144749] [PMID: 22248326]
[13]
Lee, J.; Ozcan, U. Unfolded protein response signaling and metabolic diseases. J. Biol. Chem., 2014, 289(3), 1203-1211.
[http://dx.doi.org/10.1074/jbc.R113.534743] [PMID: 24324257]
[14]
Brozzi, F.; Eizirik, D.L. ER stress and the decline and fall of pancreatic beta cells in type 1 diabetes. Ups. J. Med. Sci., 2016, 121(2), 133-139.
[http://dx.doi.org/10.3109/03009734.2015.1135217] [PMID: 26899404]
[15]
Templin, A.T.; Maier, B.; Tersey, S.A.; Hatanaka, M.; Mirmira, R.G. Maintenance of Pdx1 mRNA translation in islet β-cells during the unfolded protein response. Mol. Endocrinol., 2014, 28(11), 1820-1830.
[http://dx.doi.org/10.1210/me.2014-1157] [PMID: 25251389]
[16]
Cnop, M.; Igoillo-Esteve, M.; Cunha, D.A.; Ladrière, L.; Eizirik, D.L. An update on lipotoxic endoplasmic reticulum stress in pancreatic β-cells; Portland Press Limited, 2008.
[http://dx.doi.org/10.1042/BST0360909]
[17]
Chen, E.; Tsai, T.H.; Li, L.; Saha, P.; Chan, L.; Chang, B.H-J. PLIN2 is a Key Regulator of the Unfolded Protein Response and Endoplasmic Reticulum Stress Resolution in Pancreatic β Cells. Sci. Rep., 2017, 7, 40855.
[http://dx.doi.org/10.1038/srep40855] [PMID: 28102311]
[18]
Cha-Molstad, H.; Sung, K.S.; Hwang, J.; Kim, K.A.; Yu, J.E.; Yoo, Y.D.; Jang, J.M.; Han, D.H.; Molstad, M.; Kim, J.G.; Lee, Y.J.; Zakrzewska, A.; Kim, S.H.; Kim, S.T.; Kim, S.Y.; Lee, H.G.; Soung, N.K.; Ahn, J.S.; Ciechanover, A.; Kim, B.Y.; Kwon, Y.T. Amino-terminal arginylation targets endoplasmic reticulum chaperone BiP for autophagy through p62 binding. Nat. Cell Biol., 2015, 17(7), 917-929.
[http://dx.doi.org/10.1038/ncb3177] [PMID: 26075355]
[19]
Bromati, C.R.; Lellis-Santos, C.; Yamanaka, T.S.; Nogueira, T.C.; Leonelli, M.; Caperuto, L.C.; Gorjão, R.; Leite, A.R.; Anhê, G.F.; Bordin, S. UPR induces transient burst of apoptosis in islets of early lactating rats through reduced AKT phosphorylation via ATF4/CHOP stimulation of TRB3 expression. Am. J. Physiol. Regul. Integr. Comp. Physiol., 2011, 300(1), R92-R100.
[http://dx.doi.org/10.1152/ajpregu.00169.2010] [PMID: 21068199]
[20]
Oyadomari, S.; Takeda, K.; Takiguchi, M.; Gotoh, T.; Matsu-moto, M.; Wada, I.; Akira, S.; Araki, E.; Mori, M. Nitric ox-ide-induced apoptosis in pancreatic β cells is mediated by the endoplasmic reticulum stress pathway. Proceedings of the Na-tional Academy of sciences, 2001, pp. 10845-10850.
[21]
Pinho, A.V.; Bensellam, M.; Wauters, E.; Rees, M.; Giry-Laterriere, M.; Mawson, A.; Ly, Q.; Biankin, A.V.; Wu, J.; Laybutt, D.R.; Rooman, I. Pancreas-specific Sirt1-deficiency in mice compromises beta-cell function without development of hy-perglycemia. PLoS One, 2015, 10(6)e0128012
[http://dx.doi.org/10.1371/journal.pone.0128012] [PMID: 26046931]
[22]
Puddu, A.; Sanguineti, R.; Mach, F.; Dallegri, F.; Viviani, G.L.; Montecucco, F. Update on the protective molecular path-ways improving pancreatic beta-cell dysfunction. Mediators of Inflammation., 2013.
[23]
Meyerovich, K.; Ortis, F.; Allagnat, F.; Cardozo, A.K. Endoplasmic reticulum stress and the unfolded protein response in pancreatic islet inflammation. J. Mol. Endocrinol., 2016, 57(1), R1-R17.
[http://dx.doi.org/10.1530/JME-15-0306] [PMID: 27067637]
[24]
Kitamura, M. Endoplasmic reticulum stress and unfolded protein response in renal pathophysiology: Janus faces. Am. J. Physiol. Renal Physiol., 2008, 295(2), F323-F334.
[http://dx.doi.org/10.1152/ajprenal.00050.2008] [PMID: 18367660]
[25]
Cunard, R. Endoplasmic reticulum stress in the diabetic kidney, the good, the bad and the ugly. J. Clin. Med., 2015, 4(4), 715-740.
[http://dx.doi.org/10.3390/jcm4040715] [PMID: 26239352]
[26]
Cunard, R.; Sharma, K. The endoplasmic reticulum stress response and diabetic kidney disease. Am. J. Physiol. Renal Physiol., 2011, 300(5), F1054-F1061.
[http://dx.doi.org/10.1152/ajprenal.00021.2011] [PMID: 21345978]
[27]
Bruno, R.M.; Ghiadoni, L. Vascular smooth muscle function: Defining the diabetic vascular phenotype. Diabetologia, 2013, 56(10), 2107-2109.
[http://dx.doi.org/10.1007/s00125-013-3008-8] [PMID: 23907382]
[28]
Montero, D.; Walther, G.; Pérez-Martin, A.; Vicente-Salar, N.; Roche, E.; Vinet, A. Vascular smooth muscle function in type 2 diabetes mellitus: A systematic review and meta-analysis. Diabetologia, 2013, 56(10), 2122-2133.
[http://dx.doi.org/10.1007/s00125-013-2974-1] [PMID: 23864267]
[29]
Xie, Z.; Gong, M.C.; Su, W.; Xie, D.; Turk, J.; Guo, Z. Role of calcium-independent phospholipase A2β in high glucose-induced activation of RhoA, Rho kinase, and CPI-17 in cultured vascular smooth muscle cells and vascular smooth muscle hypercontractility in diabetic animals. J. Biol. Chem., 2010, 285(12), 8628-8638.
[http://dx.doi.org/10.1074/jbc.M109.057711] [PMID: 20086008]
[30]
Yamaguchi, H.; Igarashi, M.; Hirata, A.; Sugae, N.; Tsuchiya, H.; Jimbu, Y.; Tominaga, M.; Kato, T. Altered PDGF-BB-induced p38 MAP kinase activation in diabetic vascular smooth muscle cells: roles of protein kinase C-delta. Arterioscler. Thromb. Vasc. Biol., 2004, 24(11), 2095-2101.
[http://dx.doi.org/10.1161/01.ATV.0000144009.35400.65] [PMID: 15345514]
[31]
Navedo, M.F.; Takeda, Y.; Nieves-Cintrón, M.; Molkentin, J.D.; Santana, L.F. Elevated Ca2+ sparklet activity during acute hyperglycemia and diabetes in cerebral arterial smooth muscle cells. Am. J. Physiol. Cell Physiol., 2010, 298(2), C211-C220.
[http://dx.doi.org/10.1152/ajpcell.00267.2009] [PMID: 19846755]
[32]
Dunn, K.M.; Nelson, M.T. Calcium and diabetic vascular dysfunction. Focus on “Elevated Ca(2+) sparklet activity during acute hyperglycemia and diabetes in cerebral arterial smooth muscle cells”. Am. J. Physiol. Cell Physiol., 2010, 298(2), C203-C205.
[http://dx.doi.org/10.1152/ajpcell.00499.2009] [PMID: 19907015]
[33]
Meng, L.; Park, J.; Cai, Q.; Lanting, L.; Reddy, M.A.; Natarajan, R. Diabetic conditions promote binding of monocytes to vascular smooth muscle cells and their subsequent differentiation. Am. J. Physiol. Heart Circ. Physiol., 2010, 298(3), H736-H745.
[http://dx.doi.org/10.1152/ajpheart.00935.2009] [PMID: 20008269]
[34]
Matsumoto, T.; Kobayashi, T.; Kamata, K. Diabetic conditions act as matchmaker for monocytes and vascular smooth muscle cells. Am. J. Physiol. Heart Circ. Physiol., 2010, 298(3), H731-H733.
[http://dx.doi.org/10.1152/ajpheart.01157.2009] [PMID: 20023118]
[35]
Keller, A.C.; Knaub, L.A.; McClatchey, P.M.; Connon, C.A.; Bouchard, R.; Miller, M.W.; Geary, K.E.; Walker, L.A.; Klemm, D.J.; Reusch, J.E. Differential mitochondrial adapta-tion in primary vascular smooth muscle cells from a diabetic rat model. Oxidative medicine and cellular longevity., 2016.
[36]
Anderson, L. Six decades searching for meaning in the proteome. J. Proteomics, 2014, 107, 24-30.
[http://dx.doi.org/10.1016/j.jprot.2014.03.005] [PMID: 24642211]
[37]
Schvartz, D.; Bergsten, P.; Baek, K.H.; Barba, A. De La Rosa; Cantley J; Dayon, L; Finamore, F; Fontana, P; Gaudet, P; Goo, YA; Moulder, R; Goodlett, D; Johnson, JD; Konvalinka, A; Mulderm, H; Priego-Capote, F; Sechi, S; Snyder, M; Tiss, A; Wiederkehr, A.The Human Diabetes Proteome Project (HDPP): The 2014 update. Transl. Proteom., 2015, 8-9, 1-7.
[38]
Crèvecoeur, I.; Vig, S.; Mathieu, C.; Overbergh, L. Understanding type 1 diabetes through proteomics. Expert Rev. Proteomics, 2017, 14(7), 571-580.
[http://dx.doi.org/10.1080/14789450.2017.1345633] [PMID: 28649880]
[39]
Mannering, S.I.; Harrison, L.C.; Williamson, N.A.; Morris, J.S.; Thearle, D.J.; Jensen, K.P.; Kay, T.W.; Rossjohn, J.; Falk, B.A.; Nepom, G.T.; Purcell, A.W. The insulin A-chain epitope recognized by human T cells is posttranslationally modified. J. Exp. Med., 2005, 202(9), 1191-1197.
[http://dx.doi.org/10.1084/jem.20051251] [PMID: 16260488]
[40]
Delong, T.; Baker, R.L.; He, J.; Barbour, G.; Bradley, B.; Haskins, K. Diabetogenic T-cell clones recognize an altered peptide of chromogranin A. Diabetes, 2012, 61(12), 3239-3246.
[http://dx.doi.org/10.2337/db12-0112] [PMID: 22912420]
[41]
van Lummel, M.; Duinkerken, G.; van Veelen, P.A.; de Ru, A.; Cordfunke, R.; Zaldumbide, A.; Gomez-Touriño, I.; Arif, S.; Peakman, M.; Drijfhout, J.W.; Roep, B.O. Posttranslational modification of HLA-DQ binding islet autoantigens in type 1 diabetes. Diabetes, 2014, 63(1), 237-247.
[http://dx.doi.org/10.2337/db12-1214] [PMID: 24089515]
[42]
Marré, M.L.; Profozich, J.L.; Coneybeer, J.T.; Geng, X.; Bertera, S.; Ford, M.J.; Trucco, M.; Piganelli, J.D.; Inherent, E.R. Inherent ER stress in pancreatic islet β cells causes self-recognition by autoreactive T cells in type 1 diabetes. J. Autoimmun., 2016, 72, 33-46.
[http://dx.doi.org/10.1016/j.jaut.2016.04.009] [PMID: 27173406]
[43]
McGinty, J.W.; Chow, I.T.; Greenbaum, C.; Odegard, J.; Kwok, W.W.; James, E.A. Recognition of posttranslationally modified GAD65 epitopes in subjects with type 1 diabetes. Diabetes, 2014, 63(9), 3033-3040.
[http://dx.doi.org/10.2337/db13-1952] [PMID: 24705406]
[44]
Rondas, D.; Crèvecoeur, I.; D’Hertog, W.; Ferreira, G.B.; Staes, A.; Garg, A.D.; Eizirik, D.L.; Agostinis, P.; Gevaert, K.; Overbergh, L.; Mathieu, C. Citrullinated glucose-regulated protein 78 is an autoantigen in type 1 diabetes. Diabetes, 2015, 64(2), 573-586.
[http://dx.doi.org/10.2337/db14-0621] [PMID: 25204978]
[45]
Babon, J.A.; DeNicola, M.E.; Blodgett, D.M.; Crèvecoeur, I.; Buttrick, T.S.; Maehr, R.; Bottino, R.; Naji, A.; Kaddis, J.; Elyaman, W.; James, E.A.; Haliyur, R.; Brissova, M.; Overbergh, L.; Mathieu, C.; Delong, T.; Haskins, K.; Pugliese, A.; Campbell-Thompson, M.; Mathews, C.; Atkinson, M.A.; Powers, A.C.; Harlan, D.M.; Kent, S.C. Analysis of self-antigen specificity of islet-infiltrating T cells from human donors with type 1 diabetes. Nat. Med., 2016, 22(12), 1482-1487.
[http://dx.doi.org/10.1038/nm.4203] [PMID: 27798614]
[46]
Crèvecoeur, I.; Gudmundsdottir, V.; Vig, S.; Marques Câmara Sodré, F.; D’Hertog, W.; Fierro, A.C.; Van Lommel, L.; Gysemans, C.; Marchal, K.; Waelkens, E.; Schuit, F.; Brunak, S.; Overbergh, L.; Mathieu, C. Early differences in islets from prediabetic NOD mice: combined microarray and proteomic analysis. Diabetologia, 2017, 60(3), 475-489.
[http://dx.doi.org/10.1007/s00125-016-4191-1] [PMID: 28078386]
[47]
Wiles, T.A.; Delong, T.; Baker, R.L.; Bradley, B.; Barbour, G.; Powell, R.L.; Reisdorph, N.; Haskins, K. An insulin-IAPP hybrid peptide is an endogenous antigen for CD4 T cells in the non-obese diabetic mouse. J. Autoimmun., 2017, 78, 11-18.
[http://dx.doi.org/10.1016/j.jaut.2016.10.007] [PMID: 27802879]
[48]
Kracht, M.J.; van Lummel, M.; Nikolic, T.; Joosten, A.M.; Laban, S.; van der Slik, A.R.; van Veelen, P.A.; Carlotti, F.; de Koning, E.J.; Hoeben, R.C.; Zaldumbide, A.; Roep, B.O. Autoimmunity against a defective ribosomal insulin gene product in type 1 diabetes. Nat. Med., 2017, 23(4), 501-507.
[http://dx.doi.org/10.1038/nm.4289] [PMID: 28263308]
[49]
Burch, T.C.; Morris, M.A.; Campbell-Thompson, M.; Pugliese, A.; Nadler, J.L.; Nyalwidhe, J.O. Proteomic analysis of disease stratified human pancreas tissue indicates unique signature of type 1 diabetes. PLoS One, 2015, 10(8)e0135663
[http://dx.doi.org/10.1371/journal.pone.0135663] [PMID: 26302420]
[50]
Liu, C.W.; Atkinson, M.A.; Zhang, Q. Type 1 diabetes cadaveric human pancreata exhibit a unique exocrine tissue proteomic profile. Proteomics, 2016, 16(9), 1432-1446.
[http://dx.doi.org/10.1002/pmic.201500333] [PMID: 26935967]
[51]
Caseiro, A.; Barros, A.; Ferreira, R.; Padrão, A.; Aroso, M.; Quintaneiro, C.; Pereira, A.; Marinheiro, R.; Vitorino, R.; Amado, F. Pursuing type 1 diabetes mellitus and related complications through urinary proteomics. Transl. Res., 2014, 163(3), 188-199.
[http://dx.doi.org/10.1016/j.trsl.2013.09.005] [PMID: 24096133]
[52]
Suh, M.J.; Tovchigrechko, A.; Thovarai, V.; Rolfe, M.A.; Torralba, M.G.; Wang, J.; Adkins, J.N.; Webb-Robertson, B.J.; Osborne, W.; Cogen, F.R.; Kaplowitz, P.B.; Metz, T.O.; Nelson, K.E.; Madupu, R.; Pieper, R. Quantitative differences in the urinary prote-ome of siblings discordant for type 1 diabetes include lyso-somal enzymes. J. Proteome Res., 2015, 14(8), 3123-3135.
[http://dx.doi.org/10.1021/acs.jproteome.5b00052] [PMID: 26143644]
[53]
Singh, H.; Yu, Y.; Suh, M.J.; Torralba, M.G.; Stenzel, R.D.; Tovchigrechko, A.; Thovarai, V.; Harkins, D.M.; Rajagopala, S.V.; Osborne, W.; Cogen, F.R.; Kaplowitz, P.B.; Nelson, K.E.; Madupu, R.; Pieper, R. Type 1 Diabetes: Urinary Proteomics and Protein Network Analysis Support Perturbation of Lysosomal Function. Theranostics, 2017, 7(10), 2704-2717.
[http://dx.doi.org/10.7150/thno.19679] [PMID: 28819457]
[54]
Yohannes, E.; Chang, J.; Christ, G.J.; Davies, K.P.; Chance, M.R. Proteomics analysis identifies molecular targets related to diabetes mellitus-associated bladder dysfunction. Mol. Cell. Proteomics, 2008, 7(7), 1270-1285.
[http://dx.doi.org/10.1074/mcp.M700563-MCP200] [PMID: 18337374]
[55]
Wang, X.; Abraham, S.; McKenzie, J.A.G.; Jeffs, N.; Swire, M.; Tripathi, V.B.; Luhmann, U.F.O.; Lange, C.A.K.; Zhai, Z.; Arthur, H.M.; Bainbridge, J.; Moss, S.E.; Greenwood, J. LRG1 promotes angiogenesis by modulating endothelial TGF-β signalling. Nature, 2013, 499(7458), 306-311.
[http://dx.doi.org/10.1038/nature12345] [PMID: 23868260]
[56]
O’Donnell, L.C.; Druhan, L.J.; Avalos, B.R. Molecular characterization and expression analysis of leucine-rich alpha2-glycoprotein, a novel marker of granulocytic differentiation. J. Leukoc. Biol., 2002, 72(3), 478-485.
[PMID: 12223515]
[57]
McDermott, L.C.; Freel, J.A.; West, A.P.; Bjorkman, P.J.; Kennedy, M.W. Zn-alpha2-glycoprotein, an MHC class I-related glycoprotein regulator of adipose tissues: modification or abrogation of ligand binding by site-directed mutagenesis. Biochemistry, 2006, 45(7), 2035-2041.
[http://dx.doi.org/10.1021/bi051881v] [PMID: 16475792]
[58]
Montastier, E.; Villa-Vialaneix, N.; Caspar-Bauguil, S.; Hlavaty, P.; Tvrzicka, E.; Gonzalez, I.; Saris, W.H.; Langin, D.; Kunesova, M.; Viguerie, N. System model network for adipose tissue signatures related to weight changes in response to calorie restriction and subsequent weight maintenance. PLOS Comput. Biol., 2015, 11(1)e1004047
[http://dx.doi.org/10.1371/journal.pcbi.1004047] [PMID: 25590576]
[59]
Takahashi, E.; Unoki-Kubota, H.; Shimizu, Y.; Okamura, T.; Iwata, W.; Kajio, H.; Yamamoto-Honda, R.; Shiga, T.; Yamashita, S.; Tobe, K.; Okumura, A.; Matsumoto, M.; Yasuda, K.; Noda, M.; Kaburagi, Y. Proteomic analysis of serum biomarkers for prediabetes using the Long-Evans Agouti rat, a spontaneous animal model of type 2 diabetes mellitus. J. Diabetes Investig., 2017, 8(5), 661-671.
[http://dx.doi.org/10.1111/jdi.12638] [PMID: 28150914]
[60]
Bencharit, S.; Baxter, S.S.; Carlson, J.; Byrd, W.C.; Mayo, M.V.; Border, M.B.; Kohltfarber, H.; Urrutia, E.; Howard-Williams, E.L.; Offenbacher, S.; Wu, M.C.; Buse, J.B. Salivary proteins associated with hyperglycemia in diabetes: A proteomic analysis. Mol. Biosyst., 2013, 9(11), 2785-2797.
[http://dx.doi.org/10.1039/c3mb70196d] [PMID: 24056972]
[61]
Murri, M.; Insenser, M.; Bernal-Lopez, M.R.; Perez-Martinez, P.; Escobar-Morreale, H.F.; Tinahones, F.J. Proteomic analysis of visceral adipose tissue in pre-obese patients with type 2 diabetes. Mol. Cell. Endocrinol., 2013, 376(1-2), 99-106.
[http://dx.doi.org/10.1016/j.mce.2013.06.010] [PMID: 23791845]
[62]
McCarthy, A.M.; Spisak, K.O.; Brozinick, J.T.; Elmendorf, J.S. Loss of cortical actin filaments in insulin-resistant skeletal muscle cells impairs GLUT4 vesicle trafficking and glucose transport. Am. J. Physiol. Cell Physiol., 2006, 291(5), C860-C868.
[http://dx.doi.org/10.1152/ajpcell.00107.2006] [PMID: 16774991]
[63]
Tsakiridis, T.; Vranic, M.; Klip, A. Disassembly of the actin network inhibits insulin-dependent stimulation of glucose transport and prevents recruitment of glucose transporters to the plasma membrane. J. Biol. Chem., 1994, 269(47), 29934-29942.
[PMID: 7961991]
[64]
Janssen, M.E.; Kim, E.; Liu, H.; Fujimoto, L.M.; Bobkov, A.; Volkmann, N.; Hanein, D. Three-dimensional structure of vinculin bound to actin filaments. Mol. Cell, 2006, 21(2), 271-281.
[http://dx.doi.org/10.1016/j.molcel.2005.11.020] [PMID: 16427016]
[65]
Kiefer, F.W.; Orasanu, G.; Nallamshetty, S.; Brown, J.D.; Wang, H.; Luger, P.; Qi, N.R.; Burant, C.F.; Duester, G.; Plutzky, J. Retinaldehyde dehydrogenase 1 coordinates hepatic gluconeogenesis and lipid metabolism. Endocrinology, 2012, 153(7), 3089-3099.
[http://dx.doi.org/10.1210/en.2011-2104] [PMID: 22555438]
[66]
Kosicka, A.; Cunliffe, A.D.; Mackenzie, R.; Zariwala, M.G.; Perretti, M.; Flower, R.J.; Renshaw, D. Attenuation of plasma annexin A1 in human obesity. FASEB J., 2013, 27(1), 368-378.
[http://dx.doi.org/10.1096/fj.12-213728] [PMID: 23038751]
[67]
Cai, Q.; Li, B.; Yu, F.; Lu, W.; Zhang, Z.; Yin, M.; Gao, H. Inves-tigation of the protective effects of phlorizin on diabetic car-diomyopathy in db/db mice by quantitative proteomics. J. Diabetes Res., 2013.2013263845
[http://dx.doi.org/10.1155/2013/263845] [PMID: 23671862]
[68]
Belongie, K.J.; Ferrannini, E.; Johnson, K.; Andrade-Gordon, P.; Hansen, M.K.; Petrie, J.R. Identification of novel biomarkers to monitor β-cell function and enable early detection of type 2 diabetes risk. PLoS One, 2017, 12(8)e0182932
[http://dx.doi.org/10.1371/journal.pone.0182932] [PMID: 28846711]
[69]
Persson, F.; Rossing, P.; Hovind, P.; Stehouwer, C.D.; Schalkwijk, C.G.; Tarnow, L.; Parving, H.H. Endothelial dysfunction and inflammation predict development of diabetic nephropathy in the Irbesartan in Patients with Type 2 Diabetes and Microalbuminuria (IRMA 2) study. Scand. J. Clin. Lab. Invest., 2008, 68(8), 731-738.
[http://dx.doi.org/10.1080/00365510802187226] [PMID: 18609080]
[70]
Astrup, A.S.; Tarnow, L.; Pietraszek, L.; Schalkwijk, C.G.; Stehouwer, C.D.; Parving, H.H.; Rossing, P. Markers of endothelial dysfunction and inflammation in type 1 diabetic patients with or without diabetic nephropathy followed for 10 years: association with mortality and decline of glomerular filtration rate. Diabetes Care, 2008, 31(6), 1170-1176.
[http://dx.doi.org/10.2337/dc07-1960] [PMID: 18332153]
[71]
Agarwal, R.; Duffin, K.L.; Laska, D.A.; Voelker, J.R.; Breyer, M.D.; Mitchell, P.G. A prospective study of multiple protein biomarkers to predict progression in diabetic chronic kidney disease. Nephrol. Dial. Transplant., 2014, 29(12), 2293-2302.
[http://dx.doi.org/10.1093/ndt/gfu255] [PMID: 25085239]
[72]
Pena, M.J.; Heinzel, A.; Heinze, G.; Alkhalaf, A.; Bakker, S.J.; Nguyen, T.Q.; Goldschmeding, R.; Bilo, H.J.; Perco, P.; Mayer, B.; de Zeeuw, D.; Lambers Heerspink, H.J. A panel of novel biomarkers representing different disease pathways improves prediction of renal function decline in type 2 diabetes. PLoS One, 2015, 10(5)e0120995
[http://dx.doi.org/10.1371/journal.pone.0120995] [PMID: 25973922]
[73]
Good, D.M.; Zürbig, P.; Argilés, A.; Bauer, H.W.; Behrens, G.; Coon, J.J.; Dakna, M.; Decramer, S.; Delles, C.; Dominiczak, A.F.; Ehrich, J.H.; Eitner, F.; Fliser, D.; Frommberger, M.; Ganser, A.; Girolami, M.A.; Golovko, I.; Gwinner, W.; Haubitz, M.; Herget-Rosenthal, S.; Jankowski, J.; Jahn, H.; Jerums, G.; Julian, B.A.; Kellmann, M.; Kliem, V.; Kolch, W.; Krolewski, A.S.; Luppi, M.; Massy, Z.; Melter, M.; Neusüss, C.; Novak, J.; Peter, K.; Rossing, K.; Rupprecht, H.; Schanstra, J.P.; Schiffer, E.; Stolzenburg, J.U.; Tarnow, L.; Theodorescu, D.; Thongboonkerd, V.; Vanholder, R.; Weissinger, E.M.; Mischak, H.; Schmitt-Kopplin, P. Naturally occurring human urinary peptides for use in diagnosis of chronic kidney disease. Mol. Cell. Proteomics, 2010, 9(11), 2424-2437.
[http://dx.doi.org/10.1074/mcp.M110.001917] [PMID: 20616184]
[74]
Otu, H.H.; Can, H.; Spentzos, D.; Nelson, R.G.; Hanson, R.L.; Looker, H.C.; Knowler, W.C.; Monroy, M.; Libermann, T.A.; Karumanchi, S.A.; Thadhani, R. Prediction of diabetic nephropathy using urine proteomic profiling 10 years prior to development of nephropathy. Diabetes Care, 2007, 30(3), 638-643.
[http://dx.doi.org/10.2337/dc06-1656] [PMID: 17327333]
[75]
Merchant, M.L.; Perkins, B.A.; Boratyn, G.M.; Ficociello, L.H.; Wilkey, D.W.; Barati, M.T.; Bertram, C.C.; Page, G.P.; Rovin, B.H.; Warram, J.H.; Krolewski, A.S.; Klein, J.B. Urinary peptidome may predict renal function decline in type 1 diabetes and microalbuminuria. J. Am. Soc. Nephrol., 2009, 20(9), 2065-2074.
[http://dx.doi.org/10.1681/ASN.2008121233] [PMID: 19643930]
[76]
Schlatzer, D.; Maahs, D.M.; Chance, M.R.; Dazard, J.E.; Li, X.; Hazlett, F.; Rewers, M.; Snell-Bergeon, J.K. Novel urinary protein biomarkers predicting the development of microalbuminuria and renal function decline in type 1 diabetes. Diabetes Care, 2012, 35(3), 549-555.
[http://dx.doi.org/10.2337/dc11-1491] [PMID: 22238279]
[77]
Bhensdadia, N.M.; Hunt, K.J.; Lopes-Virella, M.F.; Michael Tucker, J.; Mataria, M.R.; Alge, J.L.; Neely, B.A.; Janech, M.G.; Arthur, J.M. Urine haptoglobin levels predict early renal functional decline in patients with type 2 diabetes. Kidney Int., 2013, 83(6), 1136-1143.
[http://dx.doi.org/10.1038/ki.2013.57] [PMID: 23536133]
[78]
Verhave, J.C.; Bouchard, J.; Goupil, R.; Pichette, V.; Brachemi, S.; Madore, F.; Troyanov, S. Clinical value of inflammatory urinary biomarkers in overt diabetic nephropathy: a prospective study. Diabetes Res. Clin. Pract., 2013, 101(3), 333-340.
[http://dx.doi.org/10.1016/j.diabres.2013.07.006] [PMID: 23880038]
[79]
Orchard, S.; Albar, J.P.; Binz, P.A.; Kettner, C.; Jones, A.R.; Salek, R.M.; Vizcaino, J.A.; Deutsch, E.W.; Hermjakob, H. Meeting new challenges: The 2014 HUPO-PSI/COSMOS Workshop: 13-15 April 2014, Frankfurt, Germany. Proteomics, 2014, 14(21-22), 2363-2368.
[http://dx.doi.org/10.1002/pmic.201470164] [PMID: 25297050]
[80]
Schutte, E.; Gansevoort, R.T.; Benner, J.; Lutgers, H.L.; Lambers Heerspink, H.J. Will the future lie in multitude? A critical appraisal of biomarker panel studies on prediction of diabetic kidney disease progression. Nephrol. Dial. Transplant., 2015, 30(Suppl. 4), iv96-iv104.
[http://dx.doi.org/10.1093/ndt/gfv119] [PMID: 26209744]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 19
ISSUE: 6
Year: 2019
Page: [732 - 743]
Pages: 12
DOI: 10.2174/1871530319666190305153810
Price: $58

Article Metrics

PDF: 34
HTML: 2
EPUB: 1
PRC: 1